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When Life Was Odd

Some 600 million years ago, a bizarre group of creatures arose. They had no heads, no tails, no eyes or mouths. They looked like nothing else that has since lived on earth. They were long thought to have been an evolutionary dead end. They may have been our ancestors.

If the history of life were a movie, you would never watch it all the way through. Soon after the opening credits you’d either fall deeply asleep or storm out in boredom. The film begins promisingly enough: it’s 4.5 billion years ago, and Earth, along with the rest of the solar system, is accreting from cosmic debris; a period of asteroid bombardment ensues-- great fx!--before the first cells make their appearance amidst the primordial ooze. But then the action dries up as the film laboriously documents more than 3 billion years of nonevents. Some cells form colonies. Others get nuclei. Hot ocean vents draw a crowd.

Maybe you’d have read the reviews, so you know there’s supposed to be a climax of sorts about 535 million years ago, when, in a relative flash called the Cambrian explosion, almost all the basic body plans of animals living today seem to evolve out of nowhere. Right away the newcomers bulk up with defensive armor and start chasing one another. That, you acknowledge, should be a pretty cool scene, but you decide it’s not worth waiting through an hour and 47 minutes of algal clots and microbial mats. Besides, you already know how the story ends.

So chances are you’d miss the brief, hallucinatory cameo by the planet’s very first large, complex life-forms. Actually, this footage probably would have been left on the cutting room floor anyway. The drama of the Ediacarans, as these organisms are known, has all the elements Hollywood abhors: ambiguity, contradiction, messy subplots, unresolved endings. Between the epochal ennui of the Precambrian (that is, before the explosion) and the abrupt spectacle of the Cambrian animals, evolution took a curious turn, creating beings so bizarre that their fossilized remains were not at first recognized as evidence of once-living things. The Ediacarans (pronounced ee-dee-ack-a-rans) are an experimental and poorly understood interlude in the evolutionary epic, the awkward adolescence of organic form: Earth’s So-Called Life.

Though virtually unknown to most audiences, the Ediacarans have been a source of scientific puzzlement since they were discovered more than a century ago. They are named for hills in southern Australia that harbor a large cache of the fossils, but Ediacaran impressions are found in rocks all over the world, from England to Africa, Russia to Canada. The fossils evoke a marine life very different from that of today’s oceans, a menagerie of feathery fronds, puckered pouches, flattened blobs, and engraved disks. They range in size from a fraction of an inch long to several feet. Many are marked with radiating, concentric, or parallel creases; others are inscribed with a filigree of delicate branches.

Even more notable are the features these organisms lack. They seem to have no heads or tails, insides or outsides, fronts or backs. They have no obvious circulatory, nervous, or digestive systems. Sans teeth, sans eyes, sans almost everything, including bones, muscles, mouths, and internal organs, the Ediacarans are nearly impossible to classify. Paleontologists cannot even agree on whether they are animal or vegetable, single-celled or multicellular. Some see in their eccentric forms the lineaments of existing animals such as mollusks, jellyfish, anemones, and worms. One investigator has argued that they are lichens. Another compares them to air mattresses.

As the earliest and oddest examples of complex life, the Ediacarans are interesting in their own right. But they are also important for understanding the extraordinary developments that succeeded them. Paleontologists once assumed that the Ediacarans had died off in a mass extinction more than half a billion years ago, well before the start of the Cambrian Period. Now, however, new fossils suggest that the twilight of the Ediacarans actually extends into the dawn of the Cambrian. Thus the Ediacarans may provide the long-sought prelude to the most significant event in life’s history. Instead of an evolutionary dead end, these otherworldly fronds, pouches, blobs, and disks may actually be ancestral portraits. And so the questions that have vexed paleontologists for decades are now more urgent than ever. When did the Ediacarans live? How did they live? And--most vexing and fundamental of all--what are they?

You need not be a paleontologist to appreciate the splendor of Mistaken Point in southeast Newfoundland. Miles from the nearest settlement and accessible only by footpaths across barren and wind-shorn moors, the point juts out into the heaving blue Atlantic, whose sculpting has exposed great ledges of dark siltstone and sandstone. On a rare day when the ledges aren’t cloaked in fog or lashed by rain or pounded by the bullying surf, the afternoon sun tilts across the canted bedrock, bringing into sharp relief scores of exotic impressions. There are fossils shaped like fern leaves, fossils like small, leafless bushes, fossils like large, lumpy coins, fossils like feathers, and one fossil that resembles a curved comb with most of its teeth missing. You don’t want to step on them, but you can’t avoid it; they’re as densely sown as wildflowers flattened in a hailstorm. They are 565 million years old.

Mistaken Point is named after the fatal errors made by sailors who mistook it for Cape Race four miles away, where ships turned north to reach the safe harbor of St. John’s. (Turn north at Mistaken Point and you crash into rocks.) But it could just as easily have been named for the errors made by geologists and paleontologists who have tried to make sense of Ediacaran fossils. When the first specimens were found in England by quarry workers in the 1860s, the disks composed of concentric rings were dismissed as some inorganic creation--possibly the result of gas bubbles percolating through ocean sediments. When German soldiers sent Ediacaran fossils home from Africa during World War I, the samples were pronounced land plants.

These mistakes were honest ones, for some Ediacaran fossils do look a bit like gas bubbles or plants. But in the mid-1940s, a geologist in South Australia stumbled on a deposit of thousands of Precambrian fossils in the Ediacara Hills that defied such facile comparisons. Here the disk and frond shapes were accompanied by a specimen reminiscent of a wad of chewing gum squashed by a densely crosshatched heel. This flat, ovoid organism, now called Dickinsonia, could be as small as the head of a tack or as large as a tablecloth. It was hard to say what it was--but it sure wasn’t a plant, and it sure wasn’t a gas bubble.

In the years following the Australian discovery, paleontologists came to accept the antiquity of the Ediacaran impressions, and they began compiling a record of similar fossils in other parts of the world. There was much head scratching and speculation as to the nature of these impressions until the 1950s. It was then that paleontologist Martin Glaessner of the University of Adelaide made the bold assertion that most of the Ediacaran organisms were the earliest members of animal families still alive today. The disk shapes he called jellyfish; the frond shapes sea pens (relatives of sea anemones). The flattened chewing-gum forms, such as Dickinsonia, were some sort of annelid--a group that now includes earthworms and leeches. They were all animals, he said, and they were precursors of extant life.

For a while, Glaessner’s thesis made sense. We had a scientific consensus on this, says geologist Mark McMenamin of Mount Holyoke College in Massachusetts. If you’d talked to the top authorities 15 years ago, there wouldn’t have been a lot of controversy.

But 14 years ago, German paleontologist Adolf Seilacher, of the University of Tübingen, took a stand contrary to Glaessner’s. None of the Ediacarans were animals, he announced; in fact, they weren’t related to anything living or long, long dead. They were single-celled beings with hydraulic architecture that could be swollen with fluid much as air mattresses are pumped full of air. The lines, rings, crosshatches, and filigreed branches that decorate Ediacaran forms were the walls of their hydraulic compartments. This architecture, Seilacher argued, let the single-celled Ediacarans increase their proportions without collapsing in on themselves. Rather than becoming multicellular--and having to invent complicated molecular signals to keep all their cells in harmony--the single-celled Ediacarans simply pumped themselves up.

To sustain themselves without a circulatory system or guts, Seilacher imagined, the Ediacarans absorbed oxygen and nutrients directly from seawater by diffusion, or perhaps they harbored symbiotic algae or bacteria that generated food for them by converting the energy in sunlight or in ocean nutrients. That would explain why so many Ediacarans were sheet- or ribbon-shaped: by maximizing the ratio of surface area to volume, they were trying to get as much exposure to seawater and sunlight as possible. An Ediacaran couldn’t be too flat or too thin.

Seilacher suggested that taxonomists give the gutless wonders of the Ediacaran a kingdom unto themselves. They weren’t animals, he said, and they weren’t plants--they weren’t even fungi or bacteria or protists (single-celled organisms such as amoebas). He called this new kingdom the vendobionta, after the Vendian Period, the last period of the Precambrian Era. And that’s when the real wrangling began. By proposing an alternative hypothesis that was consistent with the fossil evidence, Seilacher made other paleontologists realize that they had accepted Glaessner’s neat explanations too readily. Few were willing to accept Seilacher’s exotic argument wholesale; instead they began to come up with interpretations of their own. And the conjectures haven’t stopped since. After-hours at a 1992 international symposium on early life-forms, Rudolf Raff, a developmental biologist at Indiana University, decided to play a parlor game with his venerable colleagues.

I asked people, ‘What do you think these things are? What’s Dickinsonia?’ says Raff. And I got seven different answers from seven paleontologists.

Seilacher also helped overturn another of Glaessner’s cherished notions. The Australian researcher had maintained that although some of the Ediacarans might have gone extinct, many survived to evolve into the Cambrian creatures. But as paleontologists expanded their search for Precambrian fossils, the rocks themselves seemed to argue otherwise.

In sections around the world, says mit geologist John Grotzinger, you could walk up through a succession of layers that contained Ediacaran fossils, and then you wouldn’t see any Ediacaran fossils for a long, long time--I should say a great, great thickness--and then you would see the early Cambrian fossils.

Seilacher and others thus began to think of the Ediacarans as a failed experiment in life. The Cambrian animals, they argued, came from entirely different stock, perhaps tiny worms that are known only by the trails they left in Vendian mud. Many paleontologists came to believe that, animals or no, the Ediacarans had died out tens of millions of years before the Cambrian boundary and were never seen again. In fact, said some, the disappearance of the Ediacarans made the ensuing Cambrian explosion possible: only when Precambrian seas were cleared of the Ediacaran clutter could the tiny worms flourish and diversify.

But in 1994 Grotzinger and colleagues from mit and Harvard spent a summer dating rock sequences in the deserts of Namibia and found a stunning section of Ediacaran fossils running smack up against a formation from the early Cambrian. With the Ediacarans making this unexpectedly late appearance, the gap between Precambrian life-forms and the Cambrian explosion was suddenly closed.

The Namibian discovery forced researchers to reevaluate the extinction theory. Maybe the absence of Ediacarans in Cambrian rock actually resulted from the absence of conditions required for their fossilization. Cambrian creatures had shells and spines and carapaces that fossilized easily, but blobby Ediacarans were much less likely to withstand the rigors of time and geology. Perhaps because I’m a sedimentologist, says Grotzinger, I’m very sensitive to the fact that preserving these soft-bodied things is a nightmare. To leave a well-defined fossil, soft- bodied organisms must be buried rapidly, before they rot, in sediment made of particles of the right sizes. And the predators, scavengers, and burrowing creatures that suddenly appeared in the Cambrian would have made mincemeat of the mushy Ediacarans long before they had a chance to mineralize. The probability of preserving Ediacaran fossils in the Cambrian is, in my opinion, vanishingly small, says Grotzinger.

Recent discoveries of individual Ediacaran fossils in Cambrian rocks confirm Grotzinger’s opinion. Simon Conway Morris of the University of Cambridge has mulled over one of the more enigmatic fossils from the Burgess Shale of Canada--the most famous of all Cambrian fossil sites--and has decided that it is an Ediacaran holdover. University of Liverpool paleontologist Peter Crimes recently reported finding Frisbee-like Ediacaran disks in Irish rock only 510 million years old. Meanwhile, other discoveries have been pushing the beginning of Ediacaran tenure further back in time. Last year McMenamin published descriptions of new Ediacaran forms from the Sonoran Desert in Mexico that may be 600 million years old, and a team of researchers has found disks in the Canadian Rockies that are at least 610 million years old.

Experts agree that these recent finds need to be confirmed with more discoveries. Nothing is certain until you can find it in more than one place, says paleontologist Guy Narbonne of Queens University in Ontario, who helped find the disks in the Rockies. Even so, some paleontologists think that the new fossil evidence suggests a very different parable for the Precambrian-Cambrian boundary. The revised story is a kind of Glaessner-Seilacher hybrid, in which, after a long reign in the oceans, the stranger vendobionts go extinct while other Ediacarans survive into the Cambrian or even evolve into many of the marvels of that period. The ancestral status of at least some of the Ediacaran organisms is thus restored, and the magnificent, abrupt explosion of the Cambrian is reduced to a drawn-out crescendo.

Even in the revised version of the Precambrian-Cambrian transition, the Ediacarans aren’t credited with siring all the Cambrian animals. Some credit still goes to the tiny Vendian trailblazers. These creatures left winding paths that could only have been made by bodies controlled by nervous systems, and droppings that could only have been formed in guts--two features the Ediacarans lacked. It appears that the worms themselves, however, were too soft to be preserved.

And therein lies a conundrum: How could Ediacarans be any tougher than these clever worms? They had no hard parts--no teeth, no bones, no shells--and yet thousands of them fossilized under harsh conditions, often buried by currents laden with sediment or by showers of volcanic ash. A truly soft-bodied animal would have vanished without a trace under such conditions. Even the everyday environment of the Vendian seafloor could be quite punishing; one commentator described the benthic currents that battered some of the Ediacarans as the submarine equivalent of a washing machine full of sand.

The mysterious durability of the Ediacarans has troubled paleontologists for years. Glaessner himself spent some time standing on a beached jellyfish to see if it would buckle or tear under the pressure. It didn’t. Other investigators insist that the Ediacarans must have been much more thick-skinned than Glaessner’s jellyfish pedestal.

How tough were these guys? They make an impression that’s as good as a fossil log, says paleobotanist Gregory Retallack of the University of Oregon. Retallack should know--he has actually studied what happens to soft animals and tree trunks as they fossilize. Based on this comparison, and on studies of the Ediacaran fossils’ distribution and structure, Retallack thinks the Ediacarans were so tough that they couldn’t have been animals at all. Instead, he argues, the Ediacarans were lichens, those symbiotic unions of fungi and algae often seen clinging to boulders. Fungi produce a sturdy structural protein called chitin that could account for the Ediacarans’ durability.

Although Retallack’s colleagues have roundly rejected his idea-- pointing out the many differences between modern lichens and the Ediacaran fossils--he is standing his ground. They’re odd lichens; there’s nothing like them alive today, he admits, but then, they’re pretty darn odd animals as well. The ‘worms’ have no guts, the ‘jellyfish’ have muscles in the middle instead of around the bell--I mean, totally weird.

A number of researchers don’t think the Ediacarans can be lumped into any single classification. Instead they imagine the Vendian oceans inhabited by a motley crew of organisms with different life-styles and relations. Bruce Runnegar, a paleontologist at ucla, thinks Dickinsonia was probably an annelid; he says that the central line running its length might have been a gut. Other ribbed specimens, such as the sac-like Ernietta and the stalked Pteridinium, he says, may have functioned like kelp or green algae, anchored to the seafloor as they harnessed sunlight.

I think we can say for sure we haven’t got one team, says Runnegar. But how many teams we’ve got is unclear.

Some of the teams may still be with us. After some debate, paleontologists have decided that feathery fossils called Charnia and Charniodiscus were sea pens after all--as Glaessner had claimed. Other specimens have been tentatively classified as arthropods, anemones, sponges, mollusks, and seaweed. But for every similarity the Ediacarans share with living forms, there are stubborn disparities as well. There are specimens like Tribrachidium, a disk with ridges on top shaped like three joined arms, about which most experts still won’t hazard a guess. And there are specimens, like Spriggina, that seem to have an inexhaustible gestalt: the leafy Vendian has been reconstructed as a groveling annelid worm, a towering frond, and a barely three-dimensional relative of today’s horseshoe crabs and spiders.

The Ediacaran biota is something of a professional embarrassment for paleontology, says McMenamin. It’s the most dramatic moment in the history of life, and we can’t even name the cast of characters.

That uncertainty has not stopped paleontologists from conjuring visions of entire Ediacaran ecosystems--consistent, of course, with their personal vision of the individual fossils. The lichen-loving Retallack, for example, imagines a world consisting of great sponges of vegetation all over, draping the landscape. The mats of oxygen-releasing lichens could account for the rise in that atmospheric gas thought to have occurred at the end of the Precambrian, he says. They could even have provided a scaffolding for the evolution of animals. The animals needed something to live off, and in, says Retallack. They just snuggled in there and chomped away and got reproductively isolated and went through a population and evolutionary explosion. Eventually the animals cropped the Ediacaran biota back, Retallack suggests, clearing the way for terrestrial plants, which are thought to have evolved in shallow marine waters 440 million years ago.

McMenamin, on the other hand, describes a world he calls the Garden of Ediacara, in which our heroes live peaceably in the oceans, collecting sunlight and dissolved nutrients or harboring microbial colonies that do it for them. Nobody competes for anything, no one eats anybody--in fact, nobody even moves. They might be animals, but they’re just sitting on the ocean floor, photosynthesizing, says McMenamin. That would explain why they don’t have heads, or guts, or swimming muscles. They didn’t even have to move to have sex. All they had to do was release their gametes into the water.

McMenamin subscribes to the view that the apparent extinction of Ediacarans is to some degree a real one. What, then, brought trouble into paradise? He thinks the advent of mobile, predatory animals in the Cambrian might have had something to do with it. When you link brain-directed vision with predation, all hell breaks loose, says McMenamin. That’s it for the Garden of Ediacara. Cambrian organisms basically destroyed an entire ecosystem.

But other researchers blame environmental rather than ecological factors. Earth at the end of the Precambrian was a rapidly changing place. Millions of years of glaciation were coming to an end, and melting ice sheets were causing a dramatic rise in sea level; levels of oxygen in the atmosphere may have been fluctuating as well. But what might have done in the Ediacarans, according to Andrew Knoll of Harvard and his co-workers, was carbon dioxide. Based on worldwide studies of carbon isotope levels in sedimentary rocks, Knoll suspects an upwelling of deep-ocean waters released toxic levels of the gas into the shallow-sea home of the Ediacarans, killing them off while sparing the worms that would soon inherit Earth.

What’s neat about this mechanism is it predicts that organisms that exchange gases by diffusion, that have poor internal circulation, and that have low metabolic rates should be very vulnerable, says Knoll. Things that have gills, active circulation, and active metabolisms should survive. And that’s actually a nice summary distinction between the Cambrian biota and the Ediacaran biota.

Of course, Knoll admits that even these modest assumptions about Ediacaran physiology are shaky. The thing we know the least about is what we would like to know the most about--which is, what is the biology of these organisms? he says.

There are two ways to answer that question. The old-fashioned method is to go out and find more, better Ediacaran fossils. This approach still has plenty of adherents: last year, for example, Ben Waggoner of ucla and Mikhail Fedonkin of the Russian Academy of Sciences discovered a new set of fossils of an enigmatic Ediacaran called Kimberella. Although Kimberella was once thought to be a jellyfishlike creature, these new fossils show that it was more like a mollusk. Many paleontologists still dream of finding a deposit of fossils preserved with details of the tissues, or even the cells, intact. Such impressions would advance researchers’ understanding immeasurably--or, at the very least, settle the question of whether the Ediacarans were made of more than one cell.

Yet this method has its skeptics. Half of the living phyla don’t show up in the fossil record, points out Rudolf Raff. It may be that these things are gone for good and we’ll never have a clear picture of them.

Raff is a practitioner of the newfangled methods for learning more about the Ediacarans: the twin miracles of molecular phylogeny and developmental genetics. It’s possible, for example, to deduce the histories and relations of living animals by comparing their genes. Recently such analysis has suggested that the divisions between animal lineages were laid down a billion years ago--before most life-forms even had visible bodies. These Precambrian progenitors aren’t evident in the fossil record, Raff points out, because they were probably microscopic and easily wiped out.

If this new timetable is correct, then the Ediacarans appeared 400 million years after the genes for basic animal body plans had come into existence. Raff therefore suspects that the Ediacarans belonged to several different lineages that had originated hundreds of millions of years earlier. Why, then, do they all share a general, otherworldly appearance? Raff thinks that many of them evolved similar constructions independently. The Ediacarans were probably the first organisms to experiment with growing large as oxygen levels rose at the end of the Precambrian. Faced with a common challenge under common circumstances, they adopted a common solution.

The simplest way of getting morphology is to add repeating units, says Raff. You don’t have to do anything new--you just add a unit, and then add another unit, and then add another unit. And the Ediacaran creatures are built like that. These things don’t have to have a very high grade of organization. Only later, in the Cambrian, did animals manage to evolve into large sizes with the complex body plans that dominate the planet today.

Another, related way of understanding how the Ediacarans evolved is to speculate on how they grew. Evolution works its changes on animals chiefly by altering the way they develop from eggs. Thus closely related species grow in closely related patterns. Bruce Runnegar is trying to exploit this principle to figure out the affinities of the sac-shaped Ernietta. Through computer simulations, he is searching for a developmental pathway that might be expected to guide an egg to the adult Ernietta. If he succeeds, he’ll be able to compare that pathway with those of organisms alive today and look for the most similar course.

That is, if Runnegar can figure out how the Garden of Ediacara grew, he just might figure out what on Earth was growing.